Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics

Abstract

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically‐determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally‐controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause‐inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin‐like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.

Diapause-Linked Gene Expression Pattern and Related Candidate Duplicated Genes of the Mountain Butterfly Parnassius glacialis (Lepidoptera: Papilionidae) Revealed by Comprehensive Transcriptome Profiling

“…In addition, components of the pathways related to the endocrine system (e.g., GnRH, insulin, relaxin and other hormone-related signaling pathways) and the central nervous system (CNS, including cholinergic, dopaminergic, synaptic vesicle cycle and long-term potentiation) were also enriched ( Table S3 ) [ 16 , 17 , 18 ]. These KEGG pathways were mainly involved in cell proliferation, motility, immune regulation, hormone biosynthesis, neural plasticity and responses to environmental stimuli, which are necessary for insect survival, growth and longevity regulation [ 8 , 16 , 19 , 20 , 21 , 22 , 23 , 24 , 25 ]. In the CG samples, twenty-one KEGG pathways were enriched for up-regulated DEGs, including cytoskeleton, proteoglycans and immune-related pathways, in response to pathogenic infection ( Figure 2 c and Table S3 ), fifteen of which were shared with those in the NG samples.…”

Genome‐wide transcriptomic changes reveal the genetic pathways involved in insect migration

“…Likewise, CG2680 is a Haloacid Dehalogenase (HAD) family member and expressed in the ring gland, the major endocrine organ of D. melanogaster , which includes the corpus allatum responsible for producing JH (Cao et al, 2009). Also of note is the downregulation of juvenile hormone acid methyltransferase ( jhamt ) encoding the enzyme responsible for the final step in the JH biosynthesis pathway and differentially expressed between summer and fall monarch butterflies (Green & Kronforst, 2019; Shinoda & Itoyama, 2003; Zhu et al, 2009).…”

Time-Series Transcriptomic Analysis Reveals the Molecular Profiles of Diapause Termination Induced by Long Photoperiods and High Temperature in Chilo suppressalis

“…The ecdysteroid-, juvenile hormone (JH)-, and insulin/insulin-like signalling pathways regulate responses to environmental changes and are involved in diapause in many insects [ 5 , 34 ]. In pre-adult diapause, ecdysteroids (such as 20-hydroxyecdysone in insects) are generally regarded as diapause terminators [ 5 , 34 ]. Meanwhile, JH induces and maintains diapause in C. suppressalis [ 35 ].…”